Richardson started out by opening his first comic book store, Pegasus Books, in Bend, Oregon, in 1980. From there he was able to use the funds from his retail operation to start his own publishing company. Dark Horse Presents and Boris the Bear were the two initial titles in 1986 and within one year of its first publication, Dark Horse Comics added nine new titles to its roster, including The American, The Mark, Trekker, and Black Cross. Frank Miller's Sin City is one of the most famous works associated with Dark Horse, and it has become something of a token comic to the publishing house.

From 1993 to 1996, Dark Horse published a line of superhero comics under the Comics' Greatest World imprint, which was later renamed Dark Horse Heroes. After 1996, publication of this line came to a near halt, ceasing production of any books concerning the characters with the publication of the last crossover books involving Ghost, in the early 2000s.

In 2011, Dark Horse launched their iOS app and online digital comics store, followed by the release of the beta version of a native Android app in 2012. Any device with a modern web browser can be used to read Dark Horse comics at their web store.

Initiated in 1998, Dark Horse Deluxe rolled out a line of merchandise that included model kits, toys, apparel and collectibles. Its original purpose was to draw on Dark Horse properties but expanded to include such collectibles as Tim Burton's Tragic Toys for Girls and Boys, Joss Whedon's Serenity, and most recently, merchandise for the popular video-game franchise Mass Effect. Dark Horse, working with Big Tent Entertainment and the NHK broadcasting corporation, brought Domo-kun to the United States with a series of products ranging from Qee figurines to journals and stationery sets.

Dark Horse's production studio arm, Dark Horse Entertainment, produces films and television shows based on Dark Horse Comics. Established by Richardson in 1992, Dark Horse Entertainment set up shop on the lot at Twentieth Century Fox through a first-look deal with Larry Gordon and Largo Entertainment. Dark Horse Entertainment has produced over two dozen films and television projects.[8]